Brown marine algae Gongolaria baccata extract protects Caco-2 cells from oxidative stress induced by tert-butyl hydroperoxide
Introduction
A great deal of interest has been developed to isolate novel bioactive compounds from marine resources because of their numerous health beneficial effects. Marine natural products are recognized as powerful reservoirs of novel, chemically diverse molecules with wide applicability to health sciences (Tempone et al., 2011). Cystoseira C. Agardh, 1820 is a polyphyletic genus of marine macro-algae of the Sargassaceae family. Distributed along the Atlantic-Mediterranean coasts, this genus currently encompasses around 40 species (Guiry and Guiry, 2021) with several bioactivities such as antiinflammatory, antiproliferative, antioxidant (Mhadhebi et al., 2011), antifungal (Lopes et al., 2013), antibacterial (Tajbakhsh et al., 2011), antiprotozoal and antimycobacterial (Spavieri et al., 2010). The Cystoseira species have been recently reassigned into two distinct genera, namely Gongolaria and Ericaria. Cystoseira baccata (S.G. Gmelin), previously named Treptacantha baccata (S.G. Gmelin) has been finally renamed as Gongolaria baccata (S. G. Gmelin) (Molinari-Novoa and Guiry, 2020; Orellana et al., 2019). G. baccata occurs from the Baltic Sea south to the Mediterranean Sea, the Canary Islands, Mauritania and Western Sahara.
Seaweed consumption has been associated with a range of health benefits, such as anticancer, immune-modulatory, antiviral, antibacterial and antioxidant activities which are attributed to seaweed constituents, such as sulphated polysaccharides, carrageenans, fucoidans, terpenoids, polyphenols and polyunsaturated fatty acids (PUFAs) (Smit, 2004). The global production of seaweeds is mostly used for human consumption (80%), and about 20% for the hydrocolloid (agar, alginates and carrageenans) production as functional ingredients in commercial applications as stabilizers, emulsifiers, thickening agents and texture modifiers (EUMOFA, 2018). The economic potential of the algae industry is widely recognized and their bioactives have recently gained a considerable interest due to their multiple applications in the food and/or pharmaceutical industries. Chemically, the Gongolaria genus, previously assigned to Cystoseira genus, contains a wide variety of secondary metabolites, such as terpenoids, steroids, phlorotannins, phenolic compounds as well as other chemical components as, for instance, carbohydrates, triacylglycerols/fatty acids, pigments and vitamins (Bruno de Sousa et al., 2017), with radical scavenging activity (Ammar et al., 2015) and antioxidant activity (Balboa et al., 2013; Custódio et al., 2016; Mhadhebi et al., 2011, 2014). The necessity of antioxidants in food and cosmetics is evident and the search for natural alternative sources is increasing. Because of G.baccata extracts reveal to be a promising source of compounds with potential against oxidative stress, the aim of this research study was to establish if extracts of brown seaweeds (G. baccata) protect against tert-BOOH-induced oxidative stress in Caco-2 cells. As indexes of cellular oxidative stress, the generation of reactive oxygen species (ROS), the content of malondialdehyde (MDA), the activity of antioxidant/detoxification enzymes (NQO1, GST, GSH) and messenger RNA (mRNA) gene expressions linked to apoptosis/oxidative mediators were determined. Colon carcinoma (Caco-2) cells have been widely used as an in vitro model for the large intestine and are a well-established model for investigating the antioxidant effect of bioactive compounds (Phelan et al., 2009; Sambuy et al., 2005).
Section snippets
Chemicals and reagents
The compounds tert-butyl hydroperoxide (tert-BOOH), 3-[4,5 dimethylthiazol-2-yl]-2,5-diphenyl-tetrazolium bromide (MTT), menadione, dicoumarol, malondialdehyde tetrabutylammonium salt (MDA), dimethyl sulfoxide (DMSO), Dulbecco's phosphate buffered saline (DPBS, D8537), fetal bovine serum (FBS), 2-thiobarbituric acid (TBA), sodium dodecyl sulfate (SDS), β-nicotinamide adenine dinucleotide phosphate (NADPH), flavin adenine dinucleotide (FAD), bovine serum albumin (BSA), N-(2-hydroxyethyl)
Results and discussion
There is growing interest in the use of natural products to aid in the maintenance of human health. This research study demonstrates that G. baccata extract has the ability to protect human intestinal cells against oxidative insult by modulating GSH concentration, ROS generation, MDA production, antioxidant enzyme activities and apoptosis, proinflammation and oxidative stress signaling pathways.
Conclusion
In summary, our results support previous data on the antioxidant effect of G. bacatta extract. In the light of our findings, we concluded that G. baccata extract has the ability to protect human intestinal Caco-2 cells against oxidative insult by modulating GSH concentration, ROS generation, MDA production and antioxidant enzyme activities (NQO1, GST). In addition, this research study demonstrates that the GSTM2, Nrf2 and AKT1 pathways play an essential role in the mechanism underlying the
CRediT authorship contribution statement
María-Aránzazu Martínez: Conceptualization, Funding acquisition, Methodology, Validation, Formal analysis, Investigation, Writing – review & editing. Irma Ares: Investigation, Formal analysis, Writing – original draft, Writing – review & editing. Marta Martínez: Investigation, Formal analysis, Writing – original draft, Writing – review & editing. Bernardo Lopez-Torres: Methodology, Investigation. Jorge-Enrique Maximiliano: Methodology, Investigation. Jose-Luis Rodríguez: Methodology,
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This work was supported by the Project Ref. RTA2015-00010-C03 from the Ministerio de Economía, Industria y Competitividad, Spain, and Project Ref. PID 2020-15979RR-C33 from the Ministerio de Ciencia e Innovación, Spain.
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